Escherichia coli TatA and TatB proteins have N-out, C-in topology in intact cells

Journal of Biological Chemistry

Volumn 287, Issue 18, 2012, Pages 14420-14431

  Koch, Sabrina ^a   Fritsch, Maximilian J ^a   Buchanan, Grant ^a   Palmer, Tracy ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHIPATHIC; CYSTEINE RESIDUES; CYTOPLASMIC MEMBRANE; ESSENTIAL COMPONENT; FOLDED PROTEINS; INTACT CELLS; MALEIMIDES; METHOXYPOLYETHYLENE GLYCOL; N-TERMINALS; PROTEIN TRANSPORT; TAT-DEPENDENT PROTEIN TRANSPORT; THIOL REAGENTS; THYLAKOID MEMBRANES; TOPOLOGICAL ARRANGEMENT; TRANSMEMBRANE HELICES; TRANSPORT CHANNEL;

AMINO ACIDS; CELL MEMBRANES; ESCHERICHIA COLI; GLYCOLS; MACHINERY; PROTEINS;

TOPOLOGY;

CYSTEINE; ESCHERICHIA COLI PROTEIN; TWIN ARGININE PROTEIN TRANSPORT A PROTEIN; TWIN ARGININE PROTEIN TRANSPORT B PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL CELL; CARBOXY TERMINAL SEQUENCE; CYTOPLASM; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; PROTEIN TRANSPORT;

BACTERIAL SECRETION SYSTEMS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MEMBRANE TRANSPORT PROTEINS; PERIPLASM; PROTEIN STRUCTURE, SECONDARY; PROTEIN TRANSPORT;

ESCHERICHIA COLI; PROKARYOTA;

EID: 84860354294     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.354555     Document Type: Article

References (59)

1. Cline, K., and Theg, S. M. (2007) in Molecular Machines Involved in Protein Transport across Cellular Membranes (Dalbey, R. E., Koehler, C. M., and Tamanoi, F., eds) pp. 463-492, Elsevier, London
2. Palmer, T., Sargent, F., and Berks, B. C. (2010) in EcoSal-Escherichia coli and Salmonella. Cellular and Molecular Biology (Böck, A., Curtiss, R., 3rd, Kaper, J. B., Karp, P. D., Neidhardt, F. C., Nyström, T., Slauch, J. M., Squires, C. L., and Ussery, D., eds) pp. 1-73, American Society for Microbiology, Washington, D. C.
3. Berks, B. C. (1996) A common export pathway for proteins binding complex redox cofactors? Mol. Microbiol. 22, 393-404
4. Stanley, N. R., Palmer, T., and Berks, B. C. (2000) The twin arginine consensus motif of Tat signal peptides is involved in Sec-independent protein targeting in Escherichia coli. J. Biol. Chem. 275, 11591-11596 (Pubitemid 30237716)
5. Weiner, J. H., Bilous, P. T., Shaw, G. M., Lubitz, S. P., Frost, L., Thomas, G. H., Cole, J. A., and Turner, R. J. (1998) A novel and ubiquitous system for membrane targeting and secretion of cofactor-containing proteins. Cell 93, 93-101 (Pubitemid 28173555)
6. Bogsch, E. G., Sargent, F., Stanley, N. R., Berks, B. C., Robinson, C., and Palmer, T. (1998) An essential component of a novel bacterial protein export system with homologs in plastids and mitochondria. J. Biol. Chem. 273, 18003-18006 (Pubitemid 28334711)
7. Sargent, F., Bogsch, E. G., Stanley, N. R., Wexler, M., Robinson, C., Berks, B. C., and Palmer, T. (1998) Overlapping functions of components of a bacterial Sec-independent protein export pathway. EMBO J. 17, 3640-3650 (Pubitemid 28327382)
8. Sargent, F., Stanley, N. R., Berks, B. C., and Palmer, T. (1999) Sec-independent protein translocation in Escherichia coli. A distinct and pivotal role for the TatB protein. J. Biol. Chem. 274, 36073-36082
9. Jack, R. L., Sargent, F., Berks, B. C., Sawers, G., and Palmer, T. (2001) Constitutive expression of Escherichia coli tat genes indicates an important role for the twin arginine translocase during aerobic and anaerobic growth. J. Bacteriol. 183, 1801-1804 (Pubitemid 32172328)
10. Yen, M. R., Tseng, Y. H., Nguyen, E. H., Wu, L. F., and Saier, M. H., Jr. (2002) Sequence and phylogenetic analyses of the twin arginine targeting (Tat) protein export system. Arch. Microbiol. 177, 441-450 (Pubitemid 34591645)
11. Bolhuis, A., Mathers, J. E., Thomas, J. D., Barrett, C. M., and Robinson, C. (2001) TatB and TatC form a functional and structural unit of the twin arginine translocase from Escherichia coli. J. Biol. Chem. 276, 20213-20219
12. Richter, S., and Brüser, T. (2005) Targeting of unfolded PhoA to the TAT translocon of Escherichia coli. J. Biol. Chem. 280, 42723-42730 (Pubitemid 43049232)
13. Tarry, M. J., Schäfer, E., Chen, S., Buchanan, G., Greene, N. P., Lea, S. M., Palmer, T., Saibil, H. R., and Berks, B. C. (2009) Structural analysis of substrate binding by the TatBC component of the twin arginine protein transport system. Proc. Natl. Acad. Sci. U.S.A. 106, 13284-13289
14. Cline, K., and Mori, H. (2001) Thylakoid ΔpH-dependent precursor proteins bind to a cpTatC-Hcf106 complex before Tha4-dependent transport. J. Cell Biol. 154, 719-729 (Pubitemid 34292954)
15. de Leeuw, E., Granjon, T., Porcelli, I., Alami, M., Carr, S. B., Müller, M., Sargent, F., Palmer, T., and Berks, B. C. (2002) Oligomeric properties and signal peptide binding by Escherichia coli Tat protein transport complexes. J. Mol. Biol. 322, 1135-1146 (Pubitemid 35266517)
16. Alami, M., Lüke, I., Deitermann, S., Eisner, G., Koch, H. G., Brunner, J., and Müller, M. (2003) Differential interactions between a twin arginine signal peptide and its translocase in Escherichia coli. Mol. Cell 12, 937-946 (Pubitemid 37352786)
17. Gohlke, U., Pullan, L., McDevitt, C. A., Porcelli, I., de Leeuw, E., Palmer, T., Saibil, H. R., and Berks, B. C. (2005) The TatA component of the twin arginine protein transport system forms channel complexes of variable diameter. Proc. Natl. Acad. Sci. U.S.A. 102, 10482-10486 (Pubitemid 41061580)
18. Porcelli, I., de Leeuw, E., Wallis, R., van den Brink-van der Laan, E., de Kruijff, B., Wallace, B. A., Palmer, T., and Berks, B. C. (2002) Characterization and membrane assembly of the TatA component of the Escherichia coli twin arginine protein transport system. Biochemistry 41, 13690-13697 (Pubitemid 35332706)
19. Dabney-Smith, C., and Cline, K. (2009) Clustering of C-terminal stromal domains of Tha4 homo-oligomers during translocation by the Tat protein transport system. Mol. Biol. Cell 20, 2060-2069
20. Leake, M. C., Greene, N. P., Godun, R. M., Granjon, T., Buchanan, G., Chen, S., Berry, R. M., Palmer, T., and Berks, B. C. (2008) Variable stoichiometry of the TatA component of the twin arginine protein transport system observed by in vivo single-molecule imaging. Proc. Natl. Acad. Sci. U.S.A. 105, 15376-15381
21. Mori, H., and Cline, K. (2002) A twin arginine signal peptide and the pH gradient trigger reversible assembly of the thylakoid ΔpH/Tat translocase. J. Cell Biol. 157, 205-210 (Pubitemid 34839817)
22. Lee, P. A., Orriss, G. L., Buchanan, G., Greene, N. P., Bond, P. J., Punginelli, C., Jack, R. L., Sansom, M. S., Berks, B. C., and Palmer, T. (2006) Cysteine-scanning mutagenesis and disulfide mapping studies of the conserved domain of the twin arginine translocase TatB component. J. Biol. Chem. 281, 34072-34085 (Pubitemid 46036617)
23. Heijne, G. (1986) The distribution of positively charged residues in bacterial inner membrane proteins correlates with the trans-membrane topology. EMBO J. 5, 3021-3027
24. Mori, H., Summer, E. J., Ma, X., and Cline, K. (1999) Component specificity for the thylakoidal Sec and ΔpH-dependent protein transport pathways. J. Cell Biol. 146, 45-56
25. Stevenson, L. G., Strisovsky, K., Clemmer, K. M., Bhatt, S., Freeman, M., and Rather, P. N. (2007) Rhomboid protease AarA mediates quorum-sensing in Providencia stuartii by activating TatA of the twin arginine translocase. Proc. Natl. Acad. Sci. U.S.A. 104, 1003-1008 (Pubitemid 46154726)
26. Maegawa, S., Koide, K., Ito, K., and Akiyama, Y. (2007) The intramembrane active site of GlpG, an E. coli rhomboid protease, is accessible to water and hydrolyses an extramembrane peptide bond of substrates. Mol. Microbiol. 64, 435-447 (Pubitemid 46632636)
27. Wang, Y., Zhang, Y., and Ha, Y. (2006) Crystal structure of a rhomboid family intramembrane protease. Nature 444, 179-180
28. Chan, C. S., Zlomislic, M. R., Tieleman, D. P., and Turner, R. J. (2007) The TatA subunit of Escherichia coli twin arginine translocase has an N-in topology. Biochemistry 46, 7396-7404 (Pubitemid 46986366)
29. Dabney-Smith, C., Mori, H., and Cline, K. (2006) Oligomers of Tha4 organize at the thylakoid Tat translocase during protein transport. J. Biol. Chem. 281, 5476-5483 (Pubitemid 43847642)
30. Greene, N. P., Porcelli, I., Buchanan, G., Hicks, M. G., Schermann, S. M., Palmer, T., and Berks, B. C. (2007) Cysteine scanning mutagenesis and disulfide mapping studies of the TatA component of the bacterial twin arginine translocase. J. Biol. Chem. 282, 23937-23945 (Pubitemid 47328032)
31. Gouffi, K., Gérard, F., Santini, C. L., and Wu, L. F. (2004) Dual topology of the Escherichia coli TatA protein. J. Biol. Chem. 279, 11608-11615 (Pubitemid 38401662)
32. Casadaban, M. J., and Cohen, S. N. (1979) Lactose genes fused to exogenous promoters in one step using a Mu-lac bacteriophage. In vivo probe for transcriptional control sequences. Proc. Natl. Acad. Sci. U.S.A. 76, 4530-4533 (Pubitemid 9256514)
33. Wexler, M., Sargent, F., Jack, R. L., Stanley, N. R., Bogsch, E. G., Robinson, C., Berks, B. C., and Palmer, T. (2000) TatD is a cytoplasmic protein with DNase activity. No requirement for TatD family proteins in sec-independent protein export. J. Biol. Chem. 275, 16717-16722 (Pubitemid 30398902)
34. Simons, R. W., Houman, F., and Kleckner, N. (1987) Improved single and multicopy lac-based cloning vectors for protein and operon fusions. Gene 53, 85-96 (Pubitemid 17090099)
35. Sauvé, V., Bruno, S., Berks, B. C., and Hemmings, A. M. (2007) The SoxYZ complex carries sulfur cycle intermediates on a peptide swinging arm. J. Biol. Chem. 282, 23194-23204 (Pubitemid 47311913)
36. Jack, R. L., Buchanan, G., Dubini, A., Hatzixanthis, K., Palmer, T., and Sargent, F. (2004) Coordinating assembly and export of complex bacterial proteins. EMBO J. 23, 3962-3972 (Pubitemid 39472418)
37. Bartolomé, B., Jubete, Y., Martínez, E., and de la Cruz, F. (1991) Construction and properties of a family of pACYC184-derived cloning vectors compatible with pBR322 and its derivatives. Gene 102, 75-78
38. Bauer, J., Fritsch, M. J., Palmer, T., and Unden, G. (2011) Topology and accessibility of the transmembrane helices and the sensory site in the bifunctional transporter DcuB of Escherichia coli. Biochemistry 50, 5925-5938
39. Hashimoto-Gotoh, T., Yamaguchi, M., Yasojima, K., Tsujimura, A., Wakabayashi, Y., and Watanabe, Y. (2000) A set of temperature sensitive-replication/- segregation and temperature-resistant plasmid vectors with different copy numbers and in an isogenic background (chloramphenicol, kanamycin, lacZ, repA, par, and polA). Gene 241, 185-191
40. Sambrook, J., and Russell, D. W. (2001) Molecular Cloning: A Laboratory Manual, 3rd ed., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
41. Buchanan, G., de Leeuw, E., Stanley, N. R., Wexler, M., Berks, B. C., Sargent, F., and Palmer, T. (2002) Functional complexity of the twin arginine translocase TatC component revealed by site-directed mutagenesis. Mol. Microbiol. 43, 1457-1470 (Pubitemid 34595538)
42. Palmer, T., Berks, B. C., and Sargent, F. (2010) Analysis of Tat targeting function and twin arginine signal peptide activity in Escherichia coli. Methods Mol. Biol. 619, 191-216
43. Silvestro, A., Pommier, J., and Giordano, G. (1988) The inducible trimethylamine- N-oxide reductase of Escherichia coli K12. Biochemical and immunological studies. Biochim. Biophys. Acta 954, 1-13
44. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685
45. Towbin, H., Staehelin, T., and Gordon, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets. Procedure and some applications. Proc. Natl. Acad. Sci. U.S.A. 76, 4350-4354 (Pubitemid 9256559)
46. Sargent, F., Gohlke, U., De Leeuw, E., Stanley, N. R., Palmer, T., Saibil, H. R., and Berks, B. C. (2001) Purified components of the Escherichia coli Tat protein transport system form a double-layered ring structure. Eur. J. Biochem. 268, 3361-3367 (Pubitemid 32862927)
47. Wessel, D., and Flügge, U. I. (1984)Amethod for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal. Biochem. 138, 141-143 (Pubitemid 14146660)
48. Punginelli, C., Maldonado, B., Grahl, S., Jack, R., Alami, M., Schröder, J., Berks, B. C., and Palmer, T. (2007) Cysteine scanning mutagenesis and topological mapping of the Escherichia coli twin arginine translocase TatC Component. J. Bacteriol. 189, 5482-5494 (Pubitemid 47206393)
49. Lu, J., and Deutsch, C. (2001) Pegylation. A method for assessing topological accessibilities in Kv1.3. Biochemistry 40, 13288-13301 (Pubitemid 33043545)
50. Walther, T. H., Grage, S. L., Roth, N., and Ulrich, A. S. (2010) Membrane alignment of the pore-forming component TatA(d) of the twin arginine translocase from Bacillus subtilis resolved by solid-state NMR spectroscopy. J. Am. Chem. Soc. 132, 15945-15956
51. Leive, L. (1968) Studies on the permeability change produced in coliform bacteria by ethylenediaminetetraacetate. J. Biol. Chem. 243, 2373-2380
52. Berthelmann, F., Mehner, D., Richter, S., Lindenstrauss, U., Lünsdorf, H., Hause, G., and Brüser, T. (2008) Recombinant expression of tatABC and tatAC results in the formation of interacting cytoplasmic TatA tubes in Escherichia coli. J. Biol. Chem. 283, 25281-25289
53. Ize, B., Stanley, N. R., Buchanan, G., and Palmer, T. (2003) Role of the Escherichia coli Tat pathway in outer membrane integrity. Mol. Microbiol. 48, 1183-1193 (Pubitemid 36718215)
54. Bernhardt, T. G., and de Boer, P. A. (2003) The Escherichia coli amidase AmiC is a periplasmic septal ring component exported via the twin arginine transport pathway. Mol. Microbiol. 48, 1171-1182 (Pubitemid 36718214)
55. Tarry, M., Arends, S. J., Roversi, P., Piette, E., Sargent, F., Berks, B. C., Weiss, D. S., and Lea, S. M. (2009) The Escherichia coli cell division protein and model Tat substrate SufI (FtsP) localizes to the septal ring and has a multicopper oxidase-like structure. J. Mol. Biol. 386, 504-519
56. Maldonado, B., Kneuper, H., Buchanan, G., Hatzixanthis, K., Sargent, F., Berks, B. C., and Palmer, T. (2011) Characterization of the membrane-extrinsic domain of the TatB component of the twin arginine protein translocase. FEBS Lett. 585, 478-484
57. De Leeuw, E., Porcelli, I., Sargent, F., Palmer, T., and Berks, B. C. (2001) Membrane interactions and self-association of the TatA and TatB components of the twin arginine translocation pathway. FEBS Lett. 506, 143-148 (Pubitemid 32925217)
58. Hu, Y., Zhao, E., Li, H., Xia, B., and Jin, C. (2010) Solution NMR structure of the TatA component of the twin arginine protein transport system from Gram-positive bacterium Bacillus subtilis. J. Am. Chem. Soc. 132, 15942-15944
59. Bryson, K., McGuffin, L. J., Marsden, R. L., Ward, J. J., Sodhi, J. S., and Jones, D. T. (2005) Protein structure prediction servers at University College London. Nucleic Acids Res. 33, W36-W38 (Pubitemid 44529876)